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190 Guideline

Learning, techniques, and complications of


endoscopic ultrasound (EUS)-guided sampling
in gastroenterology: European Society of Gastro-
intestinal Endoscopy (ESGE) Technical Guideline

Authors M. Polkowski1, A. Larghi2, B. Weynand3, C. Boustire4, M. Giovannini5, B. Pujol6, J.-M. Dumonceau7

Institutions Institutions are listed at the end of article.

submitted 10. May 2011 This article is the second of a two-part publication yield (e. g., rapid on-site cytopathological evalua-
accepted after revision that expresses the current view of the European tion, needle diameter, microcore isolation for his-
10. October 2011
Society of Gastrointestinal Endoscopy (ESGE) topathological examination, and adequate num-
about endoscopic ultrasound (EUS)-guided sam- ber of needle passes) are discussed and recom-
Bibliography pling, including EUS-guided fine needle aspira- mendations are made for various settings, includ-
DOI http://dx.doi.org/ tion (EUS-FNA) and EUS-guided Trucut biopsy. ing solid and cystic pancreatic lesions, submuco-
10.1055/s-0031-1291543 The first part (the Clinical Guideline) focused on sal tumors, and lymph nodes. The target reader-
Published online: 16.12.2011
the results obtained with EUS-guided sampling, ship for the Clinical Guideline mostly includes
Endoscopy 2012; 44: 190205
Georg Thieme Verlag KG
and the role of this technique in patient manage- gastroenterologists, oncologists, internists, and
Stuttgart New York ment, and made recommendations on circum- surgeons while the Technical Guideline should
ISSN 0013-726X stances that warrant its use. The current Techni- be most useful to endoscopists who perform
cal Guideline discusses issues related to learning, EUS-guided sampling. A two-page executive sum-
Corresponding author
techniques, and complications of EUS-guided mary of evidence statements and recommenda-
M. Polkowski, MD
Department of
sampling, and to processing of specimens. Techni- tions is provided.
Gastroenterology, cal issues related to maximizing the diagnostic
The M. Sklodowska-Curie
Memorial Cancer Center and 1. Introduction cluded, as a minimum, endoscopic ultrasonogra-
Institute of Oncology, ! phy and words pertinent to specific key ques-
Roentgena 5 The current Technical Guideline discusses issues tions. Evidence tables were generated for each
02781 Warsaw
related to the learning, techniques, and complica- key question based on meta-analyses or random-
Poland
Fax: +48-22-5463035
tions of endoscopic ultrasound (EUS)-guided ized controlled trials (RCTs) if these were avail-
mp.polkowski@gmail.com sampling and to processing of specimens obtain- able; otherwise, case control studies, retrospec-
ed with EUS-guided fine needle aspiration (EUS- tive analyses, and case series were included. The
FNA) or EUS-guided Trucut biopsy (EUS-TCB). number of articles retrieved and selected for
The results of EUS-guided sampling in various each task force is indicated in the Evidence table
clinical indications, the role of this technique in (see " Appendix e2, available online). Evidence

patient management, and recommendations on levels and recommendation grades used in these
its use are discussed in the associated Clinical guidelines were those recommended by the
Guideline from the European Society of Gastroin- amended Scottish Intercollegiate Guidelines Net-
testinal Endoscopy (ESGE) [1]. work (SIGN) ( " Table 1) [4]. Subgroups agreed

electronically on draft proposals that were pres-


ented to the entire group for general discussion
2. Methods during two meetings held in 2010 and 2011. The
! subsequent Guideline version was discussed
The ESGE commissioned and funded this using electronic mail until unanimous agreement
Guideline. The method for guideline development was reached. Searches were re-run in February
was similar to that used for other ESGE Guidelines 2011 (this date should be taken into account for
[2, 3]. Briefly, subgroups were formed, each future updates). The final draft was approved by
charged with a series of clearly defined key ques- all members of the Guideline development group;
tions (see " Appendix e1, available online). The it was sent to all individual ESGE members in
committee chair worked with subgroup leaders April 2011 and, after incorporation of their com-
to identify pertinent search terms that always in- ments, it was endorsed by the ESGE Governing

Polkowski M et al. Learning, techniques, and complications of EUS-guided sampling Endoscopy 2012; 44: 190205
Guideline 191

of passes needed to obtain adequate results (reaching a median of 3


Table 1 Definitions of categories for evidence levels and recommendation
after 150 EUS-FNA), but no variation in severe morbidity. In all re-
grades used in this guideline [4].
ported studies, rapid on-site cytopathological examination (ROSE)
Evidence level
was used to guide the number of FNA passes needed (Evidence level
1++ High quality meta-analyses, systematic reviews of RCTs, or RCTs
with a very low risk of bias
2 +).
1+ Well conducted meta-analyses, systematic reviews of RCTs, or Trainees should demonstrate competence in linear EUS before
RCTs with a low risk of bias undertaking EUS-FNA. We discourage self-learning of EUS-FNA.
1 Meta-analyses, systematic reviews, or RCTs with a high risk of We recommend combination of the use of different simulators
bias and, if available, live pigs, during training in EUS-FNA. We recom-
2++ High quality systematic reviews of case control or cohort mend that a minimum of 20 and 30 supervised EUS-FNAs of non-
studies; high quality case control studies pancreatic and pancreatic lesions, respectively, be performed
or cohort studies with a very low risk of confounding, bias, or
with ROSE before assessment of competency in these techniques
chance and a high probability that the relationship is causal
(Recommendation grade C). ROSE is preferable although direct
2+ Well conducted case control or cohort studies with a low risk
of confounding, bias, or chance and a moderate probability that
supervision by an endosonographer experienced in EUS-FNA
the relationship is causal can be another option. Close collaboration with a cytopathologist
2 Case control or cohort studies with a high risk of confounding, experienced in evaluation of EUS-FNA samples is recommended
bias, or chance and a significant risk that the relationship is not (Recommendation grade D).
causal
3 Nonanalytic studies, e. g. case reports, case series Techniques of EUS-FNA
4 Expert opinion For EUS-FNA of pancreatic lesions the 19G, 22G and 25G needles are
Recommendation grades
characterized by similar diagnostic yields (Evidence level 1 + ) and
A At least one meta-analysis, systematic review, or RCT rated as
safety profiles (Evidence level 1 ). Although 19G needles provide a
1 + + and directly applicable to the target population
or a systematic review of RCTs
higher amount of cellular material than do thinner needles, and, if
or a body of evidence consisting principally of studies rated technically successful, offer better diagnostic yield, these advanta-
as 1 + directly applicable to the target population and demon- ges are offset by a higher rate of technical failures in the case of le-
strating overall consistency of results sions that need to be punctured from the duodenum (Evidence level
B A body of evidence including studies rated as 2 + + directly 1 ). Studies comparing EUS-FNA needles of different sizes in indi-
applicable to the target population and demonstrating overall cations other than pancreatic masses are lacking. We recommend
consistency of results
against using 19G needles for transduodenal biopsy (Recommenda-
or extrapolated evidence from studies rated as 1 + + or 1 +
tion grade C).
C A body of evidence including studies rated as 1 or 2 + directly
applicable to the target population and demonstrating overall
Applying continuous suction with a syringe during EUS-FNA improves
consistency of results the sensitivity for the diagnosis of malignancy in patients with solid
or extrapolated evidence from studies rated as 2 + + masses but not in patients with lymphadenopathy (Evidence level
D Evidence level 2 , 3 or 4 1 ). We recommend using suction for EUS-FNA of solid masses/cys-
or extrapolated evidence from studies rated as 2 + tic lesions and not using suction for EUS-FNA of lymph nodes (Re-
RCT, randomized controlled trial commendation grade C).
Using the needle stylet does not seem to impact EUS-FNA sample
quality and results (Evidence level 1 ). There is insufficient evidence
Board prior to submission to Endoscopy for international peer re- to recommend for or against using the stylet and the decision in this
view. The final revised version was approved by all members of regard should be left to the discretion of the endosonographer per-
the Guideline development group before publication. forming the procedure (Recommendation grade C).
Evidence statements and recommendations are stated in italics, Diagnostic accuracy of EUS-FNA does not differ depending on wheth-
key evidence statements and recommendations are in bold. This er the sampling is performed from the edge of a lymph node or from
Guideline will be considered for review in 2014, or sooner if im- its center (Evidence level 1 ). No data on this topic are available for
portant new evidence becomes available. Any updates to the lesions other than lymph nodes. We recommend sampling all parts
Guideline in the interim period will be noted on the ESGE web- of solid lesions or lymph nodes (Recommendation grade C) and
site: http://www.esge.com/esge-guidelines.html. sampling any solid component inside pancreatic cysts and the
wall of the cyst (Recommendation grade D).
Gross visual inspection is unreliable in assessing the adequacy of
3. Summary of statements and recommendations EUS-FNA specimens for cytopathological examination. ROSE pro-
! vides a highly reliable diagnosis with an excellent agreement with
Learning EUS-FNA the final cytopathological diagnosis (Evidence level 2 + ). There is
EUS-FNA is an extension of EUS; all endoscopists who reported their limited evidence to suggest that ROSE increases the diagnostic yield
learning curve for EUS-FNA had prior experience in EUS. Material of EUS-FNA (Evidence level 2 ). The diagnostic yield of EUS-FNA
available for learning EUS-FNA includes common didactic material with ROSE in most studies exceeds 90 %; however, similarly good re-
(e. g., books, videos), various types of simulators, and live pigs. sults have been reported from selected studies without ROSE. (Evi-
Among models available for hands-on training, live pigs are the dence level 2 + ). Data on cost effectiveness of ROSE are very lim-
most realistic and could allow the improvement of EUS-FNA skills ited. In view of these data, it is felt that implementation of ROSE
but are not widely available. The learning process of EUS-FNA has should be considered especially during the learning phase of EUS-
been studied for solid pancreatic lesions only; it showed a learning FNA and at centers in which specimen adequacy rates are below
curve with increasing sensitivity for the cytopathological diagnosis 90 % (Recommendation grade D).
of cancer (reaching 80 % after 20 30 EUS-FNA), decreasing number

Polkowski M et al. Learning, techniques, and complications of EUS-guided sampling Endoscopy 2012; 44: 190205
192 Guideline

Various studies have investigated the adequate number of needle tric EUS-TCB have similar safety profiles compared with EUS-FNA, at
passes that should be performed if ROSE is not used. Discordant least in experienced hands (Evidence level 1 ). Aspirin/nonsteroidal
conclusions have been reached for solid masses, while more concor- anti-inflammatory drugs (NSAIDs) do not seem to increase the risk
dant results have been reported for lymph nodes, liver lesions, and of bleeding following EUS-FNA (Evidence level 2 ).
pancreatic cysts. We recommend performing 3 needle passes for Antibiotic prophylaxis is recommended before EUS-guided sam-
lymph nodes and liver lesions, at least 5 needle passes for solid pan- pling of cystic lesions (Recommendation grade C) but not of solid
creatic masses, and a single pass for pancreatic cysts (Recommen- lesions (Recommendation grade B). Antibiotic prophylaxis of infec-
dation grade C). tive endocarditis is not recommended (Recommendation grade B).
Coagulation check-up is recommended before EUS-FNA only in pa-
Techniques to obtain tissue for histopathological tients with a personal or family history suggesting bleeding disor-
evaluation der or with a clear clinical indication (Recommendation grade C).
EUS-FNA with standard needles can provide tissue adequate for histo- EUS-guided sampling should not be performed in patients treated
pathological evaluation from most pancreatic tumors (Evidence level with oral anticoagulants (Recommendation grade C) or thienopyr-
2 + ). Combining EUS-FNA histology and EUS-FNA cytology seems to idines (Recommendation grade D). In addition, treatment with as-
increase EUS-FNA diagnostic yield (Evidence level 2 ) and sensitiv- pirin or NSAIDs is a contraindication for EUS-guided sampling of
ity for pancreatic cancer detection (Evidence level 2 + ). Other po- cystic lesions (Recommendation grade C).
tential advantages of EUS-FNA histology consist of facilitated im- EUS-TCB is contraindicated for lesions requiring a transduodenal
munostaining and better capability to diagnose specific tumor approach, lesions < 20 mm or of cystic appearance, and when the
types (Evidence level 2 ). We suggest implementation of this tech- operator has limited experience with standard EUS-FNA (Recom-
nique into routine practice (Recommendation grade D). mendation grade D).
Transduodenal EUS-TCB is characterized by a very high failure rate
(Evidence level 2 + ). For non-transduodenal routes, the failure rate is
low and the accuracy for the detection of malignancy is similar to 4. Learning EUS-FNA
that of EUS-FNA (Evidence level 2 + ). The accuracy of dual sampling !
(EUS-TCB + EUS-FNA) is superior to either technique alone (Evi- EUS-FNA is an extension of EUS; all endoscopists who reported their
dence level 2 + ). Sequential sampling (EUS-TCB with EUS-FNA res- learning curve for EUS-FNA had prior experience in EUS. Material
cue) has similar accuracy to that of dual sampling (Evidence level available for learning EUS-FNA includes common didactic material
2 ). EUS-TCB is superior to EUS-FNA in establishing some specific (e. g., books, videos), various types of simulators, and live pigs.
diagnoses, especially of benign tumors or if immunostaining is re- Among models available for hands-on training, live pigs are the
quired (Evidence level 2 ). In most instances EUS-TCB does not of- most realistic and could allow the improvement of EUS-FNA skills
fer advantages over EUS-FNA; however, EUS-TCB should be consid- but are not widely available. The learning process of EUS-FNA has
ered when tissue architectural details and immunostaining are re- been studied for solid pancreatic lesions only; it showed a learning
quired to establish a specific diagnosis (Recommendation grade C). curve with increasing sensitivity for the cytopathological diagnosis
of cancer (reaching 80 % after 20 30 EUS-FNA), decreasing number
Specimen processing of passes needed to obtain adequate results (reaching a median of 3
No adequate study has compared direct smear cytology vs. liquid- after 150 EUS-FNA), but no variation in severe morbidity. In all re-
based cytology (LBC) for processing specimens collected with EUS- ported studies ROSE was used to guide the number of FNA passes
FNA. Similarly, no study has evaluated which of the methods de- needed (Evidence level 2 + ).
scribed for collecting tissue fragments for histopathological exami- Trainees should demonstrate competence in linear EUS before un-
nation is better. In the case of suspected tuberculosis or lymphoma, dertaking EUS-FNA. We discourage self-learning of EUS-FNA. We
polymerase chain reaction (suspected tuberculosis) on histopatholo- recommend combination of the use of different simulators and, if
gical specimens and flow cytometry (suspected lymphoma), after available, live pigs, during training in EUS-FNA. We recommend
placement of the collected specimen in an adequate transport medi- that a minimum of 20 and 30 supervised EUS-FNA of non-pancre-
um have, been shown to significantly increase the diagnostic yield atic and pancreatic lesions, respectively, be performed with ROSE
(Evidence level 2 + ). The specific method to be used for both cytopa- before assessment of competency in these techniques (Recommen-
thological processing and collection of histopathological specimens dation grade C). ROSE is preferable although direct supervision by
should be left to the discretion of each center, depending on their an endosonographer experienced in EUS-FNA can be another op-
confidence with available methods (Recommendation grade D). tion. Close collaboration with a cytopathologist experienced in
Cell blocks can be used as a complement to rather than a replace- evaluation of EUS-FNA samples is recommended (Recommendation
ment for smears or LBC (Recommendation grade D). If tuberculosis grade D).
is suspected, then polymerase chain reaction should be used; if
lymphoma is suspected then flow cytometry should be used (Re- 4.1. Training in EUS-FNA
commendation grade C). The results of two methods for learning EUS-FNA have been re-
ported, i. e. formal training, consisting of fellowship in a dedica-
Complications of EUS-FNA and their prevention ted training center for 6 24 months, and informal training, con-
EUS-FNA is a safe procedure with a complication rate of approxi- sisting of short repeated exposures to various didactic situations
mately 1 % (Evidence level 2 + + ). Complications include infection, that usually included short hands-on experiences [5]. Formal
bleeding, and acute pancreatitis; they are more frequent for EUS- training programs are scarce in Europe and even in countries
FNA of cystic compared with solid lesions (Evidence level 2 ). Bac- where they are most developed (e. g., France), they allow training
teremia is rare after EUS-FNA, including that of perirectal and rectal of only a small number of endoscopists per year [6 8]. In addi-
lesions (Evidence level 2 + + ). The 19G, 22G, and 25G EUS-FNA needles tion, the long duration of formal training programs is impractical
present similar complication rates. Transesophageal and transgas- for the practicing, experienced endoscopist. The proportion of

Polkowski M et al. Learning, techniques, and complications of EUS-guided sampling Endoscopy 2012; 44: 190205
Guideline 193

Table 2 Series reporting the learning curve for endoscopic ultrasound (EUS)-guided fine needle aspiration (FNA) of solid pancreatic lesions.

First author, Patients/ Operator Training: type, duration Sensitivity for Complications FNAs needed to
year operators, n/n experience prior cancer diagnosis: reach 80 %
to study period First vs. last FNA sensitivity for
series compared cancer diagnosis,
n
1
Harewood, 65 /3 > 300 EUS Informal , 2 months 44 % vs. 91 % No data 20
2002 [15] < 10 EUS-FNA

Mertz, 2004 57 /1 132 EUS Informal 1, no data 50 % vs. 80 % 0 30


[14] No EUS-FNA

Eloubeidi, 2005 300 /1 316 EUS Formal, 1 year 92 % vs. 95 % 13 %2 No data


[13] 45 EUS-FNA
1
Mentoring during the performance of 2 to 10 pancreatic EUS-FNAs by an experienced endosonographer
2
Including major complications (oversedation that required the administration of a reversal agent or hospitalization or emergency department visit) in 2 % of patients

endosonographers who report that they are self-taught varies the study if applicable). ROSE may be useful to guide the number
between 8 % and 50 % [9 11]. Although unalloyed self-education of FNA passes, learn which parts of the lesion may be targeted for
is feasible for simple endoscopic procedures while maintaining increased diagnostic yield, and correct technical errors (e. g.,
high quality and safety standards [12], it has not been reported bloody or paucicellular material) [21, 22].
for more complex procedures such as EUS-FNA [5]. The American Society of Gastrointestinal Endoscopy has reap-
It seems reasonable to assume that any training has to be foun- proved in November 2008 its recommendations that competency
ded on theoretical and clinical knowledge [7]. Furthermore, all should be assessed separately for pancreatic and non-pancreatic
of the endoscopists who reported their learning curve for EUS- EUS-FNA, after at least 25 supervised procedures of each type
FNA had performed diagnostic EUS before performing supervised [16]. For all endoscopy procedures, substantial variations exist
EUS-FNA [13 15]. Competence in percutaneous abdominal ul- between individuals with regard to the speed of learning [23],
trasound is not a prerequisite for EUS or EUS-FNA because no evi- so that this number should be considered to be the minimum be-
dence was found in the literature that it improves competence in fore evaluating the trainee. In addition, as shown by Eloubeidi et
EUS. Criteria useful for assessing whether competence in EUS has al., the learning curve continues long after EUS fellowship. In a
been reached are available [16]. prospective study evaluating 300 EUS-FNA performed by a single
The use of textbooks and videos is recommended in most con- endosonographer, who had performed 45 supervised procedures
sensus statements as a basis for EUS training. Hands-on training during a training period before the study period, the proportion
in EUS-FNA has used: (i) phantoms devoid of animal material of EUS-FNA that required 5 passes significantly decreased after
(Olympus, Tokyo, Japan; self-made phantoms constructed with 100 additional procedures and the complication rate decreased
commonly available materials); (ii) models using porcine organs after 200 additional procedures (most of these complications
(upper and lower digestive EUS-FNA) [17 19]; and (iii) live pigs were graded as minor) [13].
[20]. Simulators (www.simbionix.com) do not currently offer
training in FNA. All of these models have been subjected to feasi-
bility studies only, except for the live pig model. The latter was 5. Techniques of EUS-FNA
evaluated during a 4-week EUS course: a significant improve- !
ment was noted in terms of duration and precision of the proce- Needles for sampling under EUS guidance are available from four
dure between the first and second attempt at FNA of lymph manufacturers (" Table 3). Most models are intended for aspirat-

nodes at the liver hilum [6]. This model was judged by eight EUS ing cellular material for cytopathological examination. Tissue
experts as the most realistic and useful for teaching EUS-FNA, but fragments suitable for histopathological examination can be ob-
the least easy to incorporate into fellowship training [18]. These tained using standard 19G or 22G FNA needles as well as with
experts recommended using different learning tools at different dedicated histopathological needles (e. g. Trucut, ProCore). The
time periods during the learning curve for EUS and EUS-FNA. A following sections discuss various technical issues related to
model using porcine organs was preferred over both live pigs EUS-FNA and EUS-TCB. For detailed expert instruction on how
and phantoms devoid of animal material. to perform step-by-step EUS-FNA and EUS-TCB, readers are refer-
red to other sources [24 26].
4.2. Learning curve of EUS-FNA
Five endosonographers have reported their learning curve for 5.1. Does the diameter of EUS-FNA needle matter?
EUS-FNA of solid pancreatic lesions, the procedure considered to For EUS-FNA of pancreatic lesions, the 19G, 22G and 25G needles
be the most complex (" Table 2) [13 16]. All endosonographers are characterized by similar diagnostic yields (Evidence level 1 + )
had performed a minimum of 132 300 diagnostic EUS prior to and safety profiles (Evidence level 1 ). Although 19G needles pro-
EUS-FNA, and had participated in a formal or informal training vide a higher amount of cellular material than do thinner needles,
program, and they used ROSE to guide the number of FNA passes. and, if technically successful, offer a better diagnostic yield, these
For the cytopathological diagnosis of pancreatic cancer, sensitiv- advantages are offset by a higher rate of technical failures in the
ity increased with the operators experience and reached 80 % case of lesions that need to be punctured from the duodenum (Evi-
after 20 to 30 EUS-FNA (including operators experience prior to

Polkowski M et al. Learning, techniques, and complications of EUS-guided sampling Endoscopy 2012; 44: 190205
194 Guideline

Manufacturer Model Needle type Needle diameter Single-use vs. reusable Table 3 Needles for
endoscopic ultrasound (EUS)-
Boston Scientific
guided sampling.
Expect Aspiration needle 19G, 22G, 25G Single-use
Expect Flex Aspiration needle 19G Single-use
Cook
Echotip Aspiration needle 22G Single-use
Echotip Ultra Aspiration needle 19G, 22G, 25G Single-use
Echotip ProCore 1 Aspiration needle with a core trap 19G, 22G Single-use
QuickCore Core biopsy needle 19G Single-use
EchoBrush 2 Needle with cytology brush 19G Single-use
Mediglobe
Sonotip Pro Control Aspiration needle 19G, 22G, 25G Single-use
Olympus
Power-Shot 3 Aspiration needle 22G Reusable
EZ-Shot 3 Aspiration needle 22G Single-use
EZ-Shot 2 Aspiration needle 19G, 22G, 25G Single-use
EZ-Shot 2 with sideport 4 Aspiration needle with sideport 22G Single-use
1
A newly marketed needle designed with a core trap and reverse bevel technology to increase sampling yield and promote collection of histopathological samples.
2
A modified stylet with a 1 5-mm brush at its end; it is designed to pass through a 19G EUS-FNA needle, for brushing the cyst wall.
3
Compatible exclusively with Olympus endoscopes.
4
A newly marketed needle designed with a sideport to draw tissue from both the tip and side of the needle.

dence level 1 ). Studies comparing EUS-FNA needles of different si- 5.2. Should suction be applied during EUS-FNA?
zes in indications other than pancreatic masses are lacking. Applying continuous suction with a syringe during EUS-FNA im-
We recommend against using 19G needles for transduodenal biop- proves the sensitivity for the diagnosis of malignancy in patients
sy (Recommendation grade C). with solid masses but not in patients with lymphadenopathy (Evi-
Most of the studies on EUS FNA have been conducted using 22G dence level 1 ). We recommend using suction for EUS-FNA of solid
needles. Data on thinner (25G) or larger (19G) needles are lim- masses/cystic lesions and not using suction for EUS-FNA of lymph
ited. A number of recent studies, including two RCTs, compared nodes (Recommendation grade C).
results obtained with needles of various diameters. All these Traditionally, suction is applied during EUS-FNA using a syringe
studies were performed in the setting of pancreatic masses [27 [32]. EUS-FNA without suction has been tested in an attempt to
31]. decrease sample bloodiness and to improve accuracy of micro-
It has been suggested that although thinner needles provide less scopic examination. Two RCTs have compared EUS-FNA with or
cellular material than do larger needles, the specimens from the without suction, in a total of 95 patients with suspected malig-
former are less contaminated by blood, and thus easier to inter- nant lymph nodes, pancreatic masses or submucosal tumors
pret. In addition, thinner needles may be easier to use because (SMTs) [33, 34]. In a study on 46 patients with lymphadenopathy,
of greater flexibility, particularly for locations requiring impor- applying suction did not improve diagnostic accuracy and wors-
tant scope bending [30, 31]. This preliminary evidence was only ened specimen bloodiness compared with EUS-FNA without suc-
partly confirmed in further research. tion [33]. In the other study, however, using suction during EUS-
In a small prospective, non-randomized study in 24 patients, the FNA of solid masses was associated with a significantly higher
technical success rate for the 25G needle was significantly higher sensitivity for cancer diagnosis (86 % vs. 67 %; P = 0.05) [34]. A pi-
than for the 22G needle, but only for tumors located in the unci- lot trial suggested that applying continuous high pressure suc-
nate process [29]. tion (using a balloon inflation device) allowed retrieval of tissue
An RCT in 131 patients found no significant differences between samples for histopathological examination in most cases [35].
22G and 25G needles in terms of diagnostic yield for malignancy,
number of needle passes needed to obtain a diagnosis, ease of 5.3. With or without needle stylet?
needle passage into the mass, and rates of needle malfunction Using the needle stylet does not seem to impact EUS-FNA sample
and of complications [27]. ROSE was used in this study. quality and results (Evidence level 1 ). There is insufficient evi-
Another RCT compared EUS-FNA without ROSE using 19G or 22G dence to recommend for or against using the stylet and the decision
needles in 117 patients [28]. In the intention-to-treat analysis, di- in this regard should be left to the discretion of the endosonogra-
agnostic accuracy was similar for both needles. However, if tech- pher performing the procedure (Recommendation grade C).
nical failures were excluded (per-protocol analysis), diagnostic For years the standard approach has been to reinsert the stylet
accuracy was higher with the 19G compared to the 22G needle into the needle before every pass to prevent sample contamina-
(95 % vs. 79 %, respectively; P = 0.015). Technical failures were re- tion by cells from the digestive wall as well as blockage of the
ported only for 19G needles in patients with pancreatic head needle that would hinder sample aspiration. Recently the value
masses (in 19 % of cases). The 19G needle provided a higher of this measure has been questioned by the results of three stud-
amount of cellular material with fewer passes (2.4 vs. 2.8; respec- ies, including one RCT [36 38]. While these studies found no ad-
tively; P = 0.01). No complications were observed in either group. vantages of using the stylet with regard to the quality of sample
obtained or the diagnostic yield of malignancy, they also did not
demonstrate any disadvantages of this approach. In addition, two
of these studies suffered from significant methodological limita-
tions [37 39].

Polkowski M et al. Learning, techniques, and complications of EUS-guided sampling Endoscopy 2012; 44: 190205
Guideline 195

5.4. Which part of the lesion should be punctured the slides, with the potential consequence of premature proce-
to maximize the diagnostic yield? dure termination [47].
Diagnostic accuracy of EUS-FNA does not differ depending on
whether the sampling is performed from the edge of a lymph node 5.5.2. ROSE by a cytopathologist
or from its center (Evidence level 1 ). No data on this topic are ROSE has been evaluated mostly in studies of percutaneous FNA:
available for lesions other than lymph nodes. it is generally accepted that ROSE diagnosis is highly reliable and
We recommend sampling all parts of solid lesions or lymph nodes ROSE is the critical procedure for reducing the number of inade-
(Recommendation grade C) and sampling any solid component in- quate diagnoses. In addition, ROSE may reduce costs by decreas-
side pancreatic cysts and the wall of the cyst (Recommendation ing the number of repeat procedures [48 50].
grade D). Data on ROSE of EUS-FNA specimens are limited. Based on early
Because malignant masses and lymph nodes may undergo cen- reports that suggested that ROSE may increase adequacy rates of
tral necrosis, it has been assumed that FNA of the edges of the le- EUS-FNA specimens by 10 % 29 % [51, 52], ROSE has been imple-
sion rather than of the center would increase the diagnostic mented at many EUS centers, especially in the United States [53],
yield. The study by Wallace et al. in which 46 lymph nodes were and has been used in many important studies on EUS-FNA [54
punctured found that aspiration from the edge of the lymph node 57]. The very high specimen adequacy rates consistently report-
did not increase the likelihood of a correct diagnosis when com- ed in these studies ( > 90 % 95 %) have been assumed to be linked
pared to aspiration from the lymph node center [33]. This issue to ROSE. However, EUS-FNA with vs. without ROSE has never
has not been studied for lesions other than lymph nodes. In prac- been compared in an RCT. In addition, as discussed below, there
tice, the needle is usually fanned throughout the lesion to sam- are data to suggest that neither does ROSE guarantee, nor is it es-
ple all its parts. sential to achieve high adequacy rates.
Recent research indicates that new techniques such as contrast- Evaluating ROSE accuracy or impact has been the primary focus
enhanced EUS and elastography may potentially be useful to se- of a few studies only:
lect the most suspicious area of a lymph node/tumor for EUS-FNA In a prospective study evaluating 607 EUS-FNA procedures
[40, 41]. (mostly of pancreatic masses and lymph nodes), the agree-
According to expert opinion, the diagnostic yield of EUS-FNA of ment between ROSE and final cytopathological diagnosis was
pancreatic cysts may be improved by aspirating cells from the excellent (kappa = 0.84) [58]. Compared with the true final di-
cyst wall after having aspirated cyst fluid. Using this method, Ro- agnosis, accuracies of ROSE and final cytopathological exami-
gart et al. collected cellular material adequate for cytopathologi- nation were not statistically different (93.9 % and 95.8 %,
cal assessment in 82 (76.6 %) of 107 cysts [42]. If a cyst wall thick- respectively).
ening is present (or solid nodules or a solid component inside the In a retrospective comparison of EUS-FNA results obtained by
cyst), it is advised to sample these targets before aspirating cyst one endosonographer in two university hospital centers (with
fluid (this would become more difficult once the cyst has col- ROSE available in only one of them), unequivocal cytopatholo-
lapsed). A cytology brush can also be introduced into the cyst gical diagnosis was obtained significantly more frequently
through a 19G needle to scrape the cyst wall [43 45]. This tech- (78 % vs. 52 %; odds ratio [OR], 2.94; P = 0.001) with a lower rate
nique has been shown to increase the cellular and diagnostic of unsatisfactory specimens (9 % vs. 20 %; OR, 0.36; P = 0.035) at
yields; however, serious concerns exist about its complication, the center where ROSE was available [21]. Because patient po-
in particular a high risk of intracystic bleeding [43, 45, 46]. pulations and indications for EUS-FNA significantly differed
between the compared centers, no definite conclusions can be
5.5. What is the role of ROSE? drawn from this study.
Gross visual inspection is unreliable in assessing the adequacy of In a prospective multicenter study that evaluated 409 patients,
EUS-FNA specimens for cytopathological examination. ROSE pro- two centers used ROSE whereas the other two did not [59]. The
vides a highly reliable diagnosis with an excellent agreement with results obtained in these two settings were not significantly
the final cytopathological diagnosis (Evidence level 2 + ). There is different (except for a higher negative predictive value in the
limited evidence to suggest that ROSE increases the diagnostic yield subgroup of patients with extraintestinal mass lesions when
of EUS-FNA and accuracy for malignancy detection (Evidence level ROSE was used).
2 ). The diagnostic yield of EUS-FNA with ROSE in most studies ex- In a retrospective analysis of risk factors for inadequate EUS-
ceeds 90 %; however, similarly good results have been reported from FNA specimens in 247 pancreatic tumors and 276 lymph
selected studies without ROSE. (Evidence level 2 + ). Data on cost nodes, cytopathological adequacy was significantly higher for
effectiveness of ROSE are very limited. lymph nodes (96 % vs. 84 %, P = 0.008) but not for pancreatic
In view of these data, it is felt that implementation of ROSE should tumors (99 % vs. 100 %; P = 1) when an on-site cytotechnologist
be considered especially during the learning phase of EUS-FNA and was present [60].
at centers in which specimen adequacy rates are below 90 % (Re- A recent retrospective analysis of data from a prospectively
commendation grade D). maintained database showed that in patients with solid pan-
creatic masses, ROSE reduced the number of inadequate FNA
5.5.1. Gross visual inspection of the specimen samples (1 % vs. 12.6 %; P = 0.002) and improved the sensitivity
In a prospective, double-blind, study that included 37 patients (96.2 % vs. 78.2 %; P = 0.002) and overall accuracy (96.8 % vs.
with a solid pancreatic mass, neither trained EUS technologists 86.2 %; P = 0.013) of EUS-guided FNA for the diagnosis of ma-
nor cytotechnologists were able to provide a reliable assessment lignancy. In addition, a significantly lower number of needle
of specimen adequacy by using gross visual inspection. The passes was required when ROSE was used [61]. An important
agreement between their assessment and the final microscopic limitation of this study was that patient allocation to study
assessment by a cytopathologist was only fair, with kappa values groups (95 patients biopsied with and 87 without ROSE) was
of about 0.2. False-positive assessments occurred for about 30 % of

Polkowski M et al. Learning, techniques, and complications of EUS-guided sampling Endoscopy 2012; 44: 190205
196 Guideline

not random but based on whether on-site cytopathology ser- creased from 16.7 % for the first pass to 86.7 % when more than 7
vice was available on a given day of the week. passes were performed [69]. Pellis Urquiza et al. found in a study
Of note, many recent studies in which ROSE was not used report- in 102 patients that the accuracy of EUS-FNA for pancreatic mas-
ed adequacy rates of > 90 %, indicating that at high volume centers ses reached a plateau at the 4th needle pass [65]. More recently,
ROSE is not indispensable to achieve excellent results [60, 62 Turner et al. reported in a large cohort of 559 patients with a pan-
64]. On the other hand, the use of ROSE does not unconditionally creatic mass that a diagnostic accuracy of about 80 % could be ob-
guarantee EUS-FNA success. In a survey of 21 EUS centers in the tained with only 2 to 3 needle passes [70]. A high yield with a
United States, the diagnostic rate for malignancy in patients with mean of 1.88 needle passes was also found in another study, in
pancreatic tumors varied widely from center to center, despite which the material gathered with a 22-gauge EUS-FNA needle
the fact that ROSE was used at almost all of them [53]. was first evaluated for the presence of small tissue core samples
Little is known on the impact of ROSE on EUS-FNA procedural that were placed in formalin for histopathological examination
time and it remains unclear whether using ROSE prolongs the and the rest of the material was sent for cytopathological analysis
procedure or makes it less time-consuming by reducing the [63].
number of needle passes. It is assumed that an average time for
obtaining the specimen and performing on-site examination is 5.6.2. Lymph nodes
15 min per sample [65]. Average time expenditure by the cytopa- Lymph nodes generally require a lower number of needle passes
thologist for ROSE of computed tomography (CT)-guided and ul- to obtain an adequate diagnostic accuracy. Apart from the study
trasound-guided FNA specimens is relatively high (48.7 and 44.4 by Leblanc et al. who recommended performance of at least 5
minutes, respectively; measured from the time the pathologist needle passes, other studies agreed that 3 needle passes were
left the office to the time the pathologist returned to the office sufficient [33, 52, 65, 69].
after the aspiration procedure and interpretation) [66].
5.6.3. Submucosal tumors
5.5.3. ROSE by endosonographers In the study by Pellis Urquiza et al., the accuracy of EUS-FNA for
A prospective double-blind study showed that even endosono- intramural lesions in 11 patients increased gradually with each
graphers with special training and extensive experience at re- subsequent pass to reach a plateau at the 45 % level after the
viewing cytopathological material alongside a cytopathologist fourth pass [65]. In another study, conducted in 112 patients, a
are less accurate than a cytotechnician in the assessment of speci- mean of 5.3 needle passes (range 3 9) was done, with a diagnos-
men adequacy (68 % 76 % for three endosonographers vs. 82 % tic accuracy of 83.9 % when both diagnostic and suspicious sam-
for a cytotechnician; P = 0.004) and in the diagnosis of malignancy ples were considered to be positive [71]. Differently, in a study
(69 % 72 % for three endosonographers vs. 89 % for a cytotechni- from Japan on 141 patients, a mean of 2.5 0.7 (range 1 5) pas-
cian; P < 0.001) [67]. ses were performed with an overall rate of sample adequacy of
Another study did not find significant differences in specimen 83 % that was significantly better for lesions greater than 2 cm
adequacy rates, number of needle passes or EUS-FNA perform- than for those with a smaller diameter [72]. In the latter two
ance characteristics in two subsequent 2-year periods in which studies, multivariate analysis did not show the number of needle
ROSE was performed by endosonographers (first period) or cyto- passes to be associated with the adequacy of the collected speci-
pathologists (second period). The study evaluated only a total of mens.
73 EUS-FNA procedures [68].
5.6.4. Miscellaneous and liver lesions
5.6. How many passes should be performed if ROSE The numbers of needle passes recommended for miscellaneous
is not used? and liver lesions are similar to those recommended by different
Various studies have investigated the adequate number of needle authors for pancreatic masses and lymph nodes, respectively. In
passes that should be performed if ROSE is not used. Discordant particular, Leblanc et al. found that for miscellaneous lesions the
conclusions have been reached for solid masses, while more concor- sensitivity of EUS-FNA increased from 33 % up to 92 % after 7 pas-
dant results have been reported for lymph nodes, liver lesions, and ses and did not change with additional passes [69]. For liver le-
pancreatic cysts. We recommend performing 3 needle passes for sions, Erickson et al. suggested a good diagnostic accuracy with
lymph nodes and liver lesions, at least 5 needle passes for solid pan- 2 3 needle passes, a number which is in agreement with other
creatic masses, and a single pass for pancreatic cysts (Recommen- studies [52, 73, 74].
dation grade C).
The knowledge of the adequate number of needle passes to be
performed to reach a good diagnostic accuracy is of paramount 6. Techniques to obtain tissue for histopathological
importance in centers where ROSE is not used. Differences exist evaluation
based on the nature of the target lesion. !
Although cytopathological examination of EUS-FNA specimens
5.6.1. Pancreatic masses allows detection of malignancy, it often cannot provide more
Erickson et al. found in a large study (95 patients) that a mean of specific information that may be necessary for patient manage-
3.42.2 needle passes (range, 1 10) were required to make a di- ment. Potential advantages of tissue specimens include informa-
agnosis [52]. Well-differentiated pancreatic adenocarcinomas re- tion about tissue architecture and more reliable immunostaining.
quired a higher number of passes (5.5 2.7) as compared to mod-
erately (2.7 1.2) and poorly (2.31.1) differentiated tumors. The
authors recommended performing 5 6 needle passes for pan-
creatic masses. In another study of 33 patients (9 with cystic le-
sions), Leblanc et al. found that the sensitivity gradually in-

Polkowski M et al. Learning, techniques, and complications of EUS-guided sampling Endoscopy 2012; 44: 190205
Guideline 197

Table 4 Studies in which endoscopic ultrasound-guided fine needle aspiration (EUS-FNA) with standard needles was used to obtain tissue for histopathological
evaluation (EUS-FNA histology).

First author, year (design) Indication for Patients, Needle size Specimen adequate for:
EUS-FNA n Number of
Cytology Histology Either histology or
passes, n
cytology
Moller, 2009 (retrospective) [63] Pancreatic mass 192 22G 93 % 87 % 99 %
1.88 (mean)
Iglesias-Garcia, 2007 (prospective) Pancreatic mass 62 22G 82 % 84 % 90.3 %
[77] 2 + 11
Voss, 2000 (retrospective) [79] Pancreatic mass 99 22G 74 %
2.7 (mean)
Papanikolaou, 2008 (prospective) [76] Various 2 42 22G 62 % 67 % 74 %
2 (median)
Larghi, 2005 (prospective) [35] Various 2 27 22G 96 %
Single pass 3
Turhan, 2010 (prospective) [81] Upper gastrointes- 49 22G 43 %
tinal SMTs 3 (median)
6 19G 100 %
2 (median)
Yoshida, 2009 (unclear whether GIST 49 22G 71 % 63 % 82 %
prospective or retrospective) [75] Not reported
Ando, 2002 (prospective) [82] GIST 23 22G 100 %
2.8 (mean)
Akahoshi, 2007 (prospective) [83] SMT 53 22G 79 %
2.4 (mean)
Yasuda, 2006 (prospective) [78] Lymphadenopathy 104 19G 100 %
2 median
GIST, gastrointestinal stromal tumor; SMT, submucosal tumor.
1
Two passes for cytology plus third pass for histology.
2
Mostly pancreatic mass (30 cases, 71 % [76]; and 17 cases, 63 % [35]).
3
Single pass using continuous high negative pressure suction.

6.1. Should tissue fragments be isolated from EUS-FNA trend towards higher accuracy in diagnosing specific tumor
specimens and processed for histology? types other than adenocarcinoma.
EUS-FNA with standard needles can provide tissue adequate for
histopathological evaluation from most pancreatic tumors (Evi- 6.1.2. Submucosal tumors
dence level 2 + ). Combining EUS-FNA histology and EUS-FNA cytol- Comparative data are lacking, but studies that used EUS-FNA his-
ogy seems to increase EUS-FNA diagnostic yield (Evidence level 2 ) tology alone or combined with EUS-FNA cytology reported a
and sensitivity for pancreatic cancer detection (Evidence level 2 + ). higher diagnostic yield than studies that relied only on cytopa-
Other potential advantages of EUS-FNA histology consist of facilita- thological preparations (cell blocks and especially smears) [75,
ted immunostaining and better capability to diagnose specific tu- 81 83].
mor types (Evidence level 2 ).
We suggest implementation of this technique into routine practice 6.1.3. Lymphadenopathy of unknown origin
(Recommendation grade D). In a series of 104 patients with mediastinal or/and abdominal
There is accumulating evidence that tissue adequate for histopa- lymphadenopathy of unknown origin, a specimen adequate for
thological assessment can be obtained using standard EUS-FNA histopathological evaluation was obtained in all cases using a
in a significant proportion of cases [63, 75 79]. This technique 19G needle [78]. Among 50 patients with a diagnosis of lympho-
(EUS-FNA histology) involves gross visual inspection of the sam- ma, subtyping was possible in 88 % of cases.
ple to collect minute tissue fragments that are subsequently pro-
cessed for histopathological examination (see section 7.3, below). 6.2. What is the role of EUS-guided Trucut biopsy?
EUS-FNA histology has been evaluated mostly in the setting of Transduodenal EUS-TCB is characterized by a very high failure rate
pancreatic tumors, submucosal tumors (SMTs) and lymphadeno- (Evidence level 2 + ). For non-transduodenal routes, the failure rate
pathy of unknown origin ( " Table 4). is low and the accuracy for the detection of malignancy is similar to
that of EUS-FNA (Evidence level 2 + ). The accuracy of dual sampling
6.1.1. Pancreatic mass (EUS-TCB + EUS-FNA) is superior to either technique alone (Evi-
Tissue adequate for histopathological evaluation can be obtained dence level 2 + ). Sequential sampling (EUS-TCB with EUS-FNA res-
from 67 % 86.5 % of pancreatic masses using a single pass or few cue) has similar accuracy to that of dual sampling (Evidence level
needle passes with a standard 22G needle [63, 76, 77, 79, 80]. 2 ). EUS-TCB is superior to EUS-FNA in establishing some specific
Combining EUS-FNA cytology and histology significantly increas- diagnoses, especially benign tumors or if immunostaining is requir-
es the sensitivity for malignancy diagnosis compared to cytology ed (Evidence level 2 ).
or histology alone (82.9 % vs. 68.1 % for cytology [P = 0.007], and
60 % for histology [P < 0.0001]) [63]. FNA histology also showed a

Polkowski M et al. Learning, techniques, and complications of EUS-guided sampling Endoscopy 2012; 44: 190205
198 Guideline

Table 5 Studies directly comparing endoscopic ultrasound (EUS)-guided Trucut biopsy (TCB) with EUS-guided fine needle aspiration (FNA) for detection of
malignancy.

First author, year (design) Indications for biopsy Patients, n Diagnostic accuracy for malignancy
(Sampling route)
EUS-TCB EUS-FNA1 EUS-FNA + EUS-TCB
Gerke, 2010 (prospective RCT) [90] Various 44 /36 2 88 % 78 %
(Transesophageal, transgastric,
transrectal)
Sakamoto, 2009 (prospective) [29] Pancreatic mass 24 50 % 79 %
(Transgastric, transduodenal)
Kipp, 2009 (retrospective) [94] Mediastinal/abdominal lesion 86 77 % 70 % 87 %
(Not reported)
Storch, 2008 (retrospective) [87] Mediastinal/thoracic lesions 48 79 % 79 % 98 %
(Transesophageal)
Shah, 2008 (retrospective) [95] Pancreatic mass 123 3 89 % 96 %
(Transgastric)
Aithal, 2007 (prospective) [84] Various 95 89 % 82 % 93 %
(Transesophageal, transgastric)
Saftoiu, 2007 (prospective) [86] Mediastinal masses 30 68 % 74 %
(Transesophageal)
Wittmann, 2006 (prospective) [64] Various 159 4 73 % 77 % 91 %
(Transesophageal, transgastric)
Storch, 2006 (retrospective) [88] Various 41 76 % 76 % 95 %
(Transesophageal, transgastric)
RCT, randomized controlled trial
1
EUS-FNA was performed using 22G needles in all studies. Rapid on-site cytopathological evaluation was used only in the study by Kipp et al. In the study by Gerke et al. a single pass
using high-negative suction was performed for EUS-FNA.
2
44 and 36 patients in EUS-TCB and EUS-FNA groups, respectively.
3
72 patients had only EUS-FNA and 51 patients had both EUS-FNA and EUS-TCB.
4
63 patients with lesions < 2 cm had only EUS-FNA and 96 patients with lesions 2 cm had both EUS-FNA and EUS-TCB.

In most instances EUS-TCB does not offer advantages over EUS- racy of such an approach was similar to that obtained with dual
FNA; however, EUS-TCB should be considered when tissue architec- sampling [84]. Rescue EUS-FNA was necessary only in 10 % 11 %
tural details and immunostaining are required to establish a specif- of cases in which EUS-TCB failed [84, 91]. A reverse approach
ic diagnosis (Recommendation grade C). (EUS-FNA with EUS-TCB rescue) has not been evaluated.
There is much less experience with EUS-TCB than with EUS-FNA, Although not superior to EUS-FNA in detecting malignancy, EUS-
with around 1250 EUS-TCB procedures reported to date from a TCB offers advantages in establishing some specific diagnoses, in
few centers. The 19G Quick Core needle, the only needle available particular of benign diseases [86, 87, 93]. Limited evidence sug-
for EUS-TCB, is relatively stiff and prone to malfunction when gests that immunostaining studies can be performed more reli-
biopsy is attempted in positions that require scope flexion, espe- ably on EUS-TCB than on EUS-FNA samples [89]. Promising re-
cially from the duodenum. For that reason most studies excluded sults have been reported from studies evaluating EUS-TCB in con-
patients in whom a transduodenal approach was required. The ditions in which the diagnosis relies mostly on tissue architectur-
few studies in which transduodenal EUS-TCB was attempted al details and EUS-FNA with cytopathological examination has
reported consistently very low technical success rates, ranging limited value (autoimmune pancreatitis, non-focal chronic pan-
between 8 % and 40 % in consecutive patients [29, 84, 85]. In creatitis, tuberculosis and sarcoidosis, liver parenchymal disease,
addition, most studies included only patients with target lesions lymphoma) [96 100].
20 mm [54, 86 89]. The feasibility and yield of sampling with a new histology needle
Adequacy rates reported for non-transduodenal EUS-TCB are (Echotip ProCore 19G; " Table 3) were recently evaluated in a

much higher (83 % 100 % in prospective studies) [29, 64, 84 86, multicenter study involving 109 consecutive patients with 114
90 93]. In the largest series published an adequate sample was lesions (pancreatic masses, lymph nodes and other indications)
obtained in 215 of 239 patients (90 %), with a median of 3 needle [101]. Biopsy was successful in all but two cases (98 %). A sample
passes [93]. adequate for histopathological evaluation was obtained from 89 %
In an RCT that compared EUS-TCB vs. EUS-FNA using high nega- lesions. In the remaining 9 % of cases the sample was adequate for
tive pressure, the former method provided core specimens more cytopathological evaluation (cell blocks). Sensitivity, specificity,
frequently (95.3 % vs. 27.8 %; P < 0.0001); however, this fact did positive predictive value, negative predictive value, and overall
not translate into better diagnostic accuracy (88.3 % vs. 77.8 %; P accuracy for diagnosis of malignancy were 90.2 %, 100 %, 100 %,
= 0.24) [90]. Also other studies that directly compared EUS-TCB 78.9 %, and 92.9 %, respectively. No complications were observed.
and EUS-FNA found no significant difference between these Of note, transduodenal biopsy was successful in 33 of 35 conse-
methods in the accuracy for malignancy detection ( " Table 5) cutive cases (94 %) which seems to be an important advantage
[29, 64, 84, 86 88, 90, 94, 95]. Dual sampling (EUS-FNA + EUS- over EUS-TCB. However, direct comparisons of the ProCore nee-
TCB) was consistently shown to improve accuracy when compar- dle with other needle types are lacking.
ed to either technique alone. Because using two needles in one
patient is impractical and costly, a sequential approach has been
evaluated that involved EUS-TCB with EUS-FNA rescue. The accu-

Polkowski M et al. Learning, techniques, and complications of EUS-guided sampling Endoscopy 2012; 44: 190205
Guideline 199

7. Specimen processing 7.2. Cell block


! Cell block is a preparation in which the specimen is centrifuged
No adequate study has compared direct smear cytology vs. liquid- into a pellet, formalin-fixed, paraffin-embedded, and sectioned
based cytology (LBC) for processing specimens collected with EUS- for standard staining or ancillary tests such as immunocytochem-
FNA. Similarly, no study has evaluated which of the methods de- istry and genetic analysis. Cell blocks can be prepared from left-
scribed for collecting tissue fragments for histopathological exami- over material rinsed from the needle after preparation of smears
nation is better. In the case of suspected tuberculosis or lymphoma, or from material especially obtained for this purpose (by alternat-
polymerase chain reaction (suspected tuberculosis) on histopatho- ing drops of the aspirate for smears and for cell blocks or by per-
logical specimens and flow cytometry (suspected lymphoma), after forming additional needle passes) [102]. Cell blocks are used as a
placement of the collected specimen in an adequate transport complement to rather than a replacement for smears.
medium, have been shown to significantly increase the diagnostic
yield (Evidence level 2 + ). The specific method to be used for both 7.3. Specimen processing for histology
cytopathological processing and collection of histopathological spe- Methods described for collecting tissue fragments for histopatho-
cimens should be left to the discretion of each center, depending on logical examination from specimens obtained with standard
their confidence with available methods (Recommendation grade EUS-FNA needles include injection of 2 ml saline through the
D). Cell blocks can be used as a complement to rather than a repla- needle to expel the specimen directly into a fixative [77, 79], or
cement for smears or LBC (Recommendation grade D). If tuberculo- expelling the specimen with the needle stylet onto a glass slide
sis is suspected, then polymerase chain reaction should be used; if or into saline and picking up tissue fragments to immerse them
lymphoma is suspected, then flow cytometry should be used (Re- into a fixative [63, 75]. Tumor tissue is usually whitish; however,
commendation grade C). red coagula may also contain tumor tissue [63, 75, 78]. Gross vis-
Because EUS-FNA accuracy may be compromised by inadequate ual inspection seems to be a relatively reliable way to confirm
specimens, appropriate processing of samples is crucial. Al- that the specimen is adequate for histology; however, false-posi-
though a direct smear has traditionally been used for preparing tive misinterpretation occurs in about 13.5 % 33 % of cases
EUS-FNA specimens, other methods are available including LBC, [63, 76]. Mean length of the core specimens obtained with EUS-
cell block preparation, and EUS-FNA histology. FNA is 6.5 5.3 mm (range 1 22 mm) [77]. Collecting tissue frag-
ments for EUS-FNA histology does not seem to interfere with fur-
7.1. Smears ther cytopathological evaluation of the remaining specimen [63,
Smears may be prepared using the conventional direct smear 76, 80].
method or the LBC method. Direct smears are prepared in the en- Tissue obtained with EUS-TCB is usually carefully retrieved with a
doscopy suite by extruding the needle content onto a glass slide thin injection needle from the specimen notch of the Trucut nee-
and spreading the material in an evenly thin way. This technique dle and then placed in buffered formalin and processed in the
requires a certain level of skill and practice to avoid common pit- same way as forceps biopsy specimens. Median length of core
falls, including a smear that is too thick (cells obscured within specimens obtained with EUS-TCB is 10 mm (range 2 18); one
clusters) and air-drying artifacts [102 104]. For detailed instruc- third of samples are fragmented [93]. Special care should be tak-
tion, readers are referred to recent guidelines [48]. en not to lose those tiny specimens during processing.
Smears may be allowed to dry or be fixed immediately by spray
fixation or immersion into 95 % alcohol. Unfixed smears are a po- 7.4. Special handling
tential biohazard and should be handled accordingly [48]. Air- In cases of suspected mycobacterial infection, microbiological
dried and alcohol-fixed direct smears are usually stained using confirmation should be obtained before treatment. Therefore,
Giemsa and Papanicolaou methods, respectively. Needle wash- the material from one needle pass should be reserved for specific
ings, preserved in a liquid transport medium, provide additional analysis and adequately fixed according to local protocols. Poly-
material for further studies including special stains, immunocy- merase chain reaction can be performed on paraffin-embedded
tochemistry, microbiological investigations, flow cytometry, or material obtained with EUS-guided biopsy to detect mycobacter-
molecular testing [48]. ia if the diagnosis was not suspected initially [109, 110]. Similarly,
For LBC, the aspirate is transferred into a vial containing a fixative in the case of suspected lymphoma, a specimen should be placed
or a transport medium. Smears are then prepared in the labora- in a transport medium adequate for flow cytometry, which has
tory. Importantly, the remainder of the samples should be stored been reported to significantly increase the yield for the diagnosis
so that it is available for additional preparation that may prove of lymphoma [111, 112].
useful after initial cytopathological examination. The various
available LBC methods have not been compared in EUS-FNA stud-
ies. Therefore, the specific method used should be at the discre- 8. Complications of EUS-FNA and their prevention
tion of each pathology laboratory. Thin-layer LBC is an automated !
process designed to overcome the problems associated with EUS-FNA is a safe procedure with a complication rate of approxi-
manual preparation of smears described above. This technique mately 1 % (Evidence level 2 + + ). Complications include infection,
has mostly been evaluated in cervical cytology and shown to be bleeding, and acute pancreatitis; they are more frequent for EUS-
equivalent or superior to conventional smear methods in this set- FNA of cystic compared with solid lesions (Evidence level 2 ). Bac-
ting [105]. Data on the use of thin-layer LBC preparations for EUS- teremia is rare after EUS-FNA, including that of perirectal and rec-
FNA aspirates are limited and contradictory [22, 104, 106 108]. tal lesions (Evidence level 2 + + ). The 19G, 22G, and 25G EUS-FNA
needles present similar complication rates. Transesophageal and
transgastric EUS-TCB have similar safety profiles compared with
EUS-FNA, at least in experienced hands (Evidence level 1 ). Aspir-
in/non-steroidal anti-inflammatory drugs (NSAIDs) do not seem to

Polkowski M et al. Learning, techniques, and complications of EUS-guided sampling Endoscopy 2012; 44: 190205
200 Guideline

Table 6 Complications of endoscopic ultrasound (EUS)-guided fine needle aspiration (FNA) in selected prospective series.

First author, year Patients, n Follow-up, Lost to Morbidity, Complications after EUS-FNA of: Procedure-related
days follow-up, % % mortality, %
Fluid collec- Solid masses
tions
Al-Haddad, 2008 [114] 483 30 14 1.4 3 /831 4 /400 0
Bournet, 2006 [115] 213 2 1 0 2.2 1 /74 1 4 /139 0
Eloubeidi, 2006 [117] 355 3 1 2.5 0 /0 9 /355 0
Mortensen, 2005 [113] 567 2 No data No data 0.4 0 /33 1 2 /534 0.2
Williams, 1999 [57] 333 No data No data 0.3 1 /20 1 0 /313 0
Bentz, 1998 [116] 60 No data No data 0 No data No data 0
Wiersema, 1997 [59] 457 30 0 1.1 3 /22 2 /435 0
1
Antibiotic prophylaxis administered.
2
Patients with EUS-guided interventions other than fine needle aspiration were not included in the table.

increase the risk of bleeding following EUS-FNA (Evidence level (22G vs. 25G, and 19G vs. 25G) recorded no complications at all
2 ). [27, 28]. In another study, the number of needle passes was not
Antibiotic prophylaxis is recommended before EUS-guided sam- associated with the risk of complications [119]. Given the very
pling of cystic lesions (Recommendation grade C) but not of solid low risk of EUS-FNA complications, these studies were clearly un-
lesions (Recommendation grade B). Antibiotic prophylaxis of infec- derpowered to detect a significant difference.
tive endocarditis is not recommended (Recommendation grade B). EUS-TCB presents a safety profile similar to that of EUS-FNA, at
Coagulation check-up is recommended before EUS-FNA only in pa- least in experienced hands. It has to be noted, however, that be-
tients with a personal or family history suggesting bleeding disor- cause of the limited flexibility of the Trucut needle, in most stud-
der or with a clear clinical indication (Recommendation grade C). ies EUS-TCB was not performed transduodenally. In addition,
EUS-guided sampling should not be performed in patients treated only lesions 2 cm were usually punctured. An RCT of 77 patients
with oral anticoagulants (Recommendation grade C) or thienopyr- who underwent either EUS-TCB or EUS-FNA (using a 22G needle
idines (Recommendation grade D). In addition, treatment with as- and high suction pressure) found similar complication rates in
pirin or NSAIDs is a contraindication for EUS-guided sampling of both groups (2.3 % vs. 2.8 %) [90]. Similar complication rates
cystic lesions (Recommendation grade C). (1 % 2.4 %) were reported in two large prospective series of
EUS-TCB is contraindicated for lesions requiring a transduodenal EUS-TCB including 96 and 247 patients, respectively [64, 93].
approach, and lesions < 20 mm or of cystic appearance, and when The latter study suggested that operator experience might be an
the operator has limited experience with standard EUS-FNA (Re- important factor because all complications were observed among
commendation grade D). the first 100 patients [93]. Selected small studies have reported
higher morbidity rates (4 % 12.5 %, including complications re-
8.1. What is the overall risk of complications associated quiring surgery) [26, 96,120].
with EUS-FNA?
EUS-FNA morbidity reported in the prospective series listed in 8.3. Specific complications and their prevention
" Table 6 ranged between 0 and 2.5 % (1.2 % in pooled material

from all studies); there was one death among 2468 patients 8.3.1. Infection
(0.04 %) [57, 59 ,113 117]. Complications mostly included infec- The incidence of bacteremia following EUS-FNA, including EUS-
tion, bleeding, and acute pancreatitis. Retrospective series tend FNA of rectal and perirectal lesions, is low (0 % 6 %) and similar
to under-report complications [118]. to that observed after EUS without FNA [121 124]. According to
recent guidelines, antibiotic prophylaxis is not recommended for
8.2. What are the risk factors for EUS-FNA complications? the prevention of infective endocarditis in patients with cardiac
Because complications associated with EUS FNA are very rare, risk factors who undergo EUS-FNA [125, 126].
studies would require very large numbers of patients to be ade- Clinical infectious complications after EUS-FNA of solid lesions
quately powered to evaluate risk factors for complications. (including rectal and perirectal lesions) are very rare, with inci-
Wiersema et al. reported a significantly higher incidence of com- dences of 0 % to 0.6 % in large prospective series [57, 59, 113
plications for EUS-FNA of pancreatic fluid collections than for 115, 117, 123]. As discussed above it is generally accepted that
pancreatic solid lesions (3 /22 [14 %] vs. 2 /452 [0.5 %], respective- the higher risk of EUS-FNA in fluid collections warrants antibiotic
ly; P < 0.001). The complications observed after FNA of fluid col- prophylaxis. Fluoroquinolones administered intravenously be-
lections included two febrile episodes and one pseudocyst he- fore the procedure and orally for 3 5 days thereafter are prob-
morrhage; two of these patients required surgery [59]. In all sub- ably the regimen used most commonly [114, 125]; betalactam
sequent studies ( " Table 6), antibiotic prophylaxis was adminis- antibiotics have also been used in this setting [115, 119]. The in-
tered before EUS-FNA of pancreatic fluid collections, but in spite cidence of infectious complications in prospective studies that
of that the overall morbidity remained higher than for solid mas- used prophylaxis was low (0 % to 1.4 %) [57, 113 115]. In a large
ses (5 /210 [2.4 %] vs. 10 /1386 [0.7 %], respectively). Based on retrospective analysis of 603 patients with 651 pancreatic cysts, a
these data, a cystic character of the lesion is considered a risk fac- single patient (0.2 %) developed infection [127].
tor for complications, both of infection and bleeding. EUS-FNA of mediastinal cysts may be complicated by infection,
A larger needle size does not seem to be associated with a higher including life-threatening mediastinitis [26, 128, 129]. For that
complication risk. Two RCTs comparing needles of different sizes reason, and because of limited clinical impact, EUS-FNA of simple

Polkowski M et al. Learning, techniques, and complications of EUS-guided sampling Endoscopy 2012; 44: 190205
Guideline 201

mediastinal cystic lesions is usually considered to be contraindi- rombotic agents for endoscopic procedures, readers are referred
cated [130, 131]. On the other hand, EUS-FNA might be of value in to specific guidelines) [139, 140].
atypical/complex mediastinal cystic lesions to rule out malignan-
cy. In such cases antibiotic prophylaxis should be administered 8.3.3. Acute pancreatitis
[132]. The reported incidence of acute pancreatitis after EUS-FNA of
pancreatic lesions ranged from 0.26 % in a large multicenter sur-
8.3.2. Bleeding vey study to 2 % in a prospective study that specifically searched
Clinically significant bleeding is a possible, but very rare compli- for this complication in 100 consecutive patients [117, 118, 134,
cation of EUS-FNA. Only single cases have been reported, includ- 141]. Among the 14 cases analyzed in the multicenter survey,
ing one that was fatal [113]. The incidence reported in large pro- pancreatitis was mild, moderate, and severe in 10 (71 %), 3 (21
spective series ranged between 0 % and 0.5 % [57, 59, 113 115, %), and 1 (7 %) case, respectively. The median duration of hospita-
117]. Self-limited intraprocedural bleeding with no clinical con- lization for treatment of pancreatitis was 3 days (range 1 21
sequences is more common. Extraluminal bleeding (visible as an days). One patient (7 %) with multiple comorbid conditions died
expanding echopoor region adjacent to the sampled lesion) has as a result of pancreatitis [118]. Factors suggested to predispose
been reported to occur during 1.3 % 2.6 % of procedures [133, to post-EUS-FNA pancreatitis included a history of recent pan-
134], and intracystic bleeding (gradually expanding hyperechoic creatitis and puncture of a benign pancreatic lesion; however, a
area within the cyst) during 6 % of EUS-FNA of pancreatic cysts significant relationship was not demonstrated [118, 141].
[135]. In both instances the management consisted in cessation
of further needle passes, observation by EUS, and a short course 8.3.4. Other complications
of antibiotics to prevent infection [133, 135]. The clinical course Less frequent complications include esophageal or duodenal per-
has been uneventful in all cases. Rare cases of intraprocedural lu- foration [59, 113, 115], bile peritonitis after FNA of obstructed bile
minal bleeding requiring intervention (adrenaline injection and ducts or the gallbladder [142], and seeding of tumorous cells
hemostatic clips) have been described [134]. The true effective- along the needle tract [143, 144]. The rate of cervical esophagus
ness of the above measures used in the management of extra- perforation at the time of intubation with a curvilinear echoen-
luminal or intraluminal bleeding related to EUS-FNA has not doscope is 0.06 %, as assessed in a large prospective study [145].
been investigated. The perforation risk is higher in stenotic tumors and aggressive
Although not evidence-based, platelet count and coagulation attempts at passing the stenosis with the endoscope should be a-
check-up are performed before EUS-FNA in most centers, with voided [113]. Bile peritonitis frequently requires surgery and has
platelet count < 50000 /mm3 and international normalized ratio been reported after inadvertent biliary puncture during EUS-FNA
> 1.5 considered to be contraindications to EUS-guided sampling aggravated by subsequent endoscopic retrograde cholangiopan-
[43, 114, 130, 136]. Criticisms of this approach include poor sensi- creatography [142]. Three cases of tumor seeding following
tivity and specificity for the prediction of postintervention bleed- EUS-FNA have been reported to date [144, 146, 147]; a retrospec-
ing, costs, and the risk that it might indeed increase rather than tive study suggests that peritoneal carcinomatosis related to pan-
decrease the risk of litigation [137]. Recent guidelines recom- creas cancer may occur more frequently after percutaneous com-
mend the taking of a bleeding history including detail of family pared to EUS-guided FNA [148].
history, previous excessive post-traumatic or postsurgical bleed-
ing and use of antithrombotic drugs, and performance of coagu-
lation testing only in patients with a positive history or a clear Note
clinical indication (e. g., liver disease) [137]. !
Data on EUS-guided sampling in patients undergoing treatment ESGE guidelines represent a consensus of best practice based on
with antithrombotic agents are limited. A prospective controlled the available evidence at the time of preparation. They may not
study found no increased bleeding risk following EUS-FNA in 26 apply in all situations and should be interpreted in the light of
patients taking aspirin or NSAIDS when compared to 190 con- specific clinical situations and resource availability. Further con-
trols (overall bleeding rates of 0 % and 3.7 % respectively) [134]. trolled clinical studies may be needed to clarify aspects of these
Two of six patients (33 %) on a prophylactic dose of low-molecu- statements, and revision may be necessary as new data appear.
lar weight heparin (LMWH) had clinically non-significant bleed- Clinical consideration may justify a course of action at variance
ing episodes. Based on these data, and according to published to these recommendations. ESGE guidelines are intended to be
guidelines, the authors recommended that if EUS-guided sam- an educational device to provide information that may assist en-
pling has to be performed in a patient on LMWH, the procedure doscopists in providing care to patients. They are not rules and
should be performed 8 hours or more after administration of the should not be construed as establishing a legal standard of care
drug [134, 138]. No data on the risk of EUS-guided sampling in or as encouraging, advocating, requiring, or discouraging any
patients treated with thienopyridines are available. particular treatment.
EUS-guided sampling should not be performed in patients taking
oral anticoagulants [139]. According to a recently issued ESGE Alberto Larghi and Marc Giovannini have received research sup-
guideline on endoscopy and antiplatelet agents (APA), EUS-FNA port from Cook Endoscopy Inc., Limerick, Ireland.
of solid masses can be performed in patients taking aspirin or
NSAIDS, but not in patients taking thienopyridines (e. g. clopido-
grel). EUS-FNA of cystic lesions should not be performed in pa-
tients taking APA of any kind [140]. If a change in antithrombotic
therapy is required for performance of EUS-FNA, the throm-
boembolic risk in a given patient and the risk-to-benefit ratio
should be considered (for details on the management of antith-

Polkowski M et al. Learning, techniques, and complications of EUS-guided sampling Endoscopy 2012; 44: 190205
202 Guideline

Institutions 21 Klapman JB, Logrono R, Dye CE et al. Clinical impact of on-site cytopa-
1
Department of Gastroenterology and Hepatology, Medical Centre for Post- thology interpretation on endoscopic ultrasound-guided fine needle
graduate Education and Department of Gastroenterology, The M. Sklodows- aspiration. Am J Gastroenterol 2003; 98: 1289 1294
ka-Curie Memorial Cancer Center and Institute of Oncology, Warsaw, Poland 22 LeBlanc JK, Emerson RE, Dewitt J et al. A prospective study comparing
2
Digestive Endoscopy Unit, Universita Cattolica del Sacro Cuore, Rome, Italy rapid assessment of smears and ThinPrep for endoscopic ultrasound-
3
CHU Mont-Godinne, Universit catholique de Louvain, Yvoir, Belgium guided fine-needle aspirates. Endoscopy 2010; 42: 389 394
4
Department of Digestive Endoscopy, Hpital Saint Joseph, Marseille, France 23 Sarker SK, Albrani T, Zaman A et al. Procedural performance in gastro-
5
Endoscopic Unit, Paoli-Calmettes Institut, Marseille, France
6 intestinal endoscopy: live and simulated. World J Surg 2010; 34:
Department of Gastroenterology, Hpital Priv Jean Mermoz, Lyon, France
7 1764 1770
Service of Gastroenterology and Hepatology, Geneva University Hospitals,
Geneva, Switzerland 24 Vilmann P, Saftoiu A. Endoscopic ultrasound-guided fine needle aspira-
tion biopsy: equipment and technique. J Gastroenterol Hepatol 2006;
21: 1646 1655
Acknowledgment 25 Wiersema MJ, Levy MJ, Harewood GC et al. Initial experience with EUS-
! guided trucut needle biopsies of perigastric organs. Gastrointest En-
The authors thank Dr. Genevive Ranchin-Monges for helpful dosc 2002; 56: 275 278
26 Varadarajulu S, Fraig M, Schmulewitz N et al. Comparison of EUS-guid-
comments.
ed 19-gauge Trucut needle biopsy with EUS-guided fine-needle as-
piration. Endoscopy 2004; 36: 397 401
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Guideline 205

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Appendix 1 and 2 are available online:

online content viewable at:


www.thieme-connect.de/ejournals/abstract/endoscopy/
doi/10.1055/s-0031-1291543

Polkowski M et al. Learning, techniques, and complications of EUS-guided sampling Endoscopy 2012; 44: 190205

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